Clearance of Vibrio campbellii injected into the hemolymph of Callinectes sapidus, the Atlantic blue crab: The effects of prior exposure to bacteria and environmental hypoxia

Fish and Shellfish Immunology

Volumn 25, Issue 6, 2008, Pages 718-730

  Macey, Brett M ^a   Rathburn, Charles K ^a   Thibodeaux, Lindy K ^a   Burnett, Louis E ^a   Burnett, Karen G ^a  

^a School of Business   (United States)

Author keywords

Bacterial clearance; Blue crab; Callinectes sapidus; Hemocyte; Hemolymph; Hypercapnic hypoxia; Immune response; Quantitative real time PCR; Vibrio

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); CALLINECTES SAPIDUS; CRUSTACEA; DECAPODA (CRUSTACEA); VIBRIO; VIBRIO CAMPBELLII;

EID: 54949150492     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2008.02.009     Document Type: Article

References (57)

1. Noga E.J., Arroll T.A., and Zhiqin F. Specificity and some physicochemical characteristics of the antibacterial activity from blue crab Callinectes sapidus. Fish Shellfish Immunol 6 (1996) 403-412
2. Welsh P.C., and Sizemore R.K. Incidence of bacteremia in stressed and unstressed populations of the blue crab, Callinectes sapidus. Appl Environ Microbiol 50 (1985) 420-425
3. Fuhrman J.A. Marine viruses and their biogeochemical and ecological effects. Nature 399 (1999) 541-548
4. Davis J.W., and Sizemore R.K. Incidence of Vibrio species associated with blue crabs (Callinectes sapidus) collected from Galveston Bay, Texas. Appl Environ Microbiol 43 (1982) 1092-1097
5. Burnett L.E., Holman J.D., Jorgensen D.D., Ikerd J.L., and Burnett K.G. Immune defense reduces respiratory fitness in Callinectes sapidus, the Atlantic blue crab. Biol Bull 211 (2006) 50-57
6. Scholnick D.A., Burnett K.G., and Burnett L.E. Impact of exposure to bacteria on metabolism in the penaeid shrimp Litopenaeus vannamei. Biol Bull 211 (2006) 44-49
7. Kurtz J., and Franz K. Innate defence: evidence for memory in invertebrate immunity. Nature 425 (2003) 37-38
8. Moret Y., and Siva-Jothy M.T. Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc R Soc Lond B 270 (2003) 2475-2480
9. Hauton C., Brockton V., and Smith V.J. Changes in immune gene expression and resistance to bacterial infection in lobster (Homarus gammarus) post-larval stage VI following acute or chronic exposure to immune stimulating compounds. Mol Immunol 44 (2007) 443-450
10. Martin G.G., Hose J.E., Minka G., and Rosenberg S. Clearance of bacteria injected into the hemolymph of the ridgeback prawn, Sicyonia ingentis (Crustacea: Decapoda): role of hematopoietic tissue. J Morphol 227 (1996) 227-233
11. Clem L.W., Clem K., and McCumber L. Recognition of xenogeneic proteins by the blue crab: dissociation of the clearance and degradation reactions and lack of involvement of circulating hemocytes and humoral factors. Dev Comp Immunol 8 (1984) 31-40
12. Martin G.G., Poole D., Poole C., Hose J.E., Arias M., Reynolds L., et al. Clearance of bacteria injected into the hemolymph of the penaeid shrimp, Sicyonia ingentis. J Invertebr Pathol 62 (1993) 308-315
13. Holman J.D., Burnett K.G., and Burnett L.E. Effects of hypercapnic hypoxia on the clearance of Vibrio campbellii in the Atlantic blue crab, Callinectes sapidus Rathbun. Biol Bull 206 (2004) 188-196
14. Burgents J.E., Burnett L.E., Stabb E.V., and Burnett K.G. Localization and bacteriostasis of Vibrio introduced into the Pacific white shrimp, Litopenaeus vannamei. Dev Comp Immunol 29 (2005) 681-691
15. Sritunyalucksana K., Gangnonngiw W., Archakunakorn S., Fegan D., and Flegel T.W. Bacterial clearance rate and a new differential hemocyte staining method to assess immunostimulant activity in shrimp. Dis Aquat Org 63 (2005) 89-94
16. Burge E.J., Madigan D.J., Burnett L.E., and Burnett K.G. Lysozyme gene expression by hemocytes of Pacific white shrimp, Litopenaeus vannamei, after injection with Vibrio. Fish Shellfish Immunol 22 (2007) 327-339
17. Smith V.J., and Ratcliffe N.A. Host defense reactions of the shore crab, Carcinus maenas (L.): clearance and distribution of injected test particles. J Mar Biol Assoc U K 60 (1980) 89-102
18. Iwanaga S., and Lee B.L. Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38 (2005) 128-150
19. Johansson M.W., Keyser P., Sritunyalucksana K., and Söderhäll K. Crustacean haemocytes and haematopoiesis. Aquaculture 191 (2000) 45-52
20. Muñoz M., Cedeño R., Rodríguez J., van der Knaap W.P.W., Mialhe E., and Bachère E. Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeus vannamei. Aquaculture 191 (2000) 89-107
21. Söderhäll I., Bangyeekhun E., Mayo S., and Söderhäll K. Hemocyte production and maturation in an invertebrate animal; proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus. Dev Comp Immunol 27 (2003) 661-672
22. Söderhäll K., and Cerenius L. Crustacean immunity. Annu Rev Fish Dis 2 (1992) 3-23
23. White K.N., Ratcliffe N.A., and Rossa M. The antibacterial activity of haemocyte clumps in the gills of the shore crab, Carcinus maenas. J Mar Biol Assoc U K 65 (1985) 857-870
24. Tanner C.A., Burnett L.E., and Burnett K.G. The effects of hypoxia and pH on phenoloxidase activity in the Atlantic blue crab, Callinectes sapidus. Comp Biochem Physiol A Mol Int Physiol 144 (2006) 218-223
25. Boleza K.A., Burnett L.E., and Burnett K.G. Hypercapnic hypoxia compromises bactericidal activity of fish anterior kidney cells against opportunistic environmental pathogens. Fish Shellfish Immunol 11 (2001) 593-610
26. Boyd J.N., and Burnett L.E. Reactive oxygen intermediate production by oyster hemocytes exposed to hypoxia. J Exp Biol 202 (1999) 3135-3143
27. Burgents J.E., Burnett K.G., and Burnett L.E. Effects of hypoxia and hypercapnic hypoxia on the localization and the elimination of Vibrio campbellii in Litopenaeus vannamei, the Pacific white shrimp. Biol Bull 208 (2005) 159-168
28. Mikulski C.M., Burnett L.E., and Burnett K.G. The effects of hypercapnic hypoxia on the survival of shrimp challenged with Vibrio parahaemolyticus. J Shellfish Res 19 (2000) 301-311
29. Booth C.E., McMahon B.R., and Pinder A.W. Oxygen uptake and the potentiating effects of increased hemolymph lactate on oxygen transport during exercise in the blue crab Callinectes sapidus. J Comp Physiol 148 (1982) 111-121
30. 14C-thiocyanate. Comp Biochem Physiol A 56 (1977) 411-413
31. van de Braak C.B., Botterblom M.H., Taverne N., van Muiswinkel W.B., Rombout J.H., and van der Knaap W.P. The roles of haemocytes and the lymphoid organ in the clearance of injected Vibrio bacteria in Penaeus monodon shrimp. Fish Shellfish Immunol 13 (2002) 293-309
32. White K.N., and Ratcliffe N.A. The segregation and elimination of radio-fluorescent-labeled marine bacteria from the haemolymph of the shore crab, Carcinus maenas. J Mar Biol Assoc U K 64 (1982) 557-570
33. Sung H.H., and Song Y.L. Tissue location of Vibrio antigen delivered by immersion to tiger shrimp (Penaeus monodon). Aquaculture 145 (1996) 41-54
34. Martin G.G., Quintero M., Quigley M., and Khosrovian H. Elimination of sequestered material from the gills of decapod crustaceans. J Crust Biol 20 (2000) 209-217
35. Merrill D.P., Mongeon S.A., and Fisher S. Distribution of fluorescent latex particles following clearance from the hemolymph of the freshwater crayfish Orconectes virilis (Hagen). J Comp Physiol 132 (1979) 363-368
36. Smith V.J., and Ratcliffe N.A. Pathological changes in the nephrocytes of the shore crab, Carcinus maenas, following injection of bacteria. J Invertebr Pathol 38 (1981) 113-121
37. Smith V.J., and Ratcliffe N.A. Cellular defense reactions of the shore crab, Carcinus maenas: in vivo hemocytic and histopathological responses to injected bacteria. J Invertebr Pathol 35 (1980) 65-74
38. Destoumieux D., Muñoz M., Cosseau C., Rodriguez J., Bulet P., Comps M., et al. Penaeidins, antimicrobial peptides with chitin-binding activity, are produced and stored in shrimp granulocytes and released after microbial challenge. J Cell Sci 113 (2000) 461-469
39. Hauton C., Brockton V., and Smith V.J. Cloning of a crustin-like, single whey-acidic-domain, antibacterial peptide from the haemocytes of the European lobster, Homarus gammarus, and its response to infection with bacteria. Mol Immunol 43 (2006) 1490-1496
40. Song Y.L., and Hsieh Y.T. Immunostimulation of tiger shrimp (Penaeus monodon) hemocytes for generation of microbicidal substances: analysis of reactive oxygen species. Dev Comp Immunol 18 (1994) 201-209
41. Khoo L., Robinette D.W., and Noga E.J. Callinectin, an antibacterial peptide from blue crab, Callinectes sapidus, hemocytes. Mar Biotechnol 1 (1999) 44-51
42. Stensvag K., Haug T., Sperstad S.V., Rekdal O., Indrevoll B., Styrvold O.B., et al. A proline-arginine-rich antimicrobial peptide isolated from the spider crab, Hyas araneus. Dev Comp Immunol 32 (2008) 275-285
43. Relf J.M., Chisholm J.R.S., Kemp G.D., and Smith V.J. Purification and characterization of a cysteine-rich 11.5-kDa antibacterial protein from the granular haemocytes of the shore crab, Carcinus maenas. Eur J Biochem 264 (1999) 350-357
44. Schnapp D., Kemp G.D., and Smith V.J. Purification and characterization of a proline-rich antibacterial peptide, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas. Eur J Biochem 240 (1996) 532-539
45. Sritunyalucksana K., and Söderhäll K. The proPO and clotting system in crustaceans. Aquaculture 191 (2000) 53-69
46. Destoumieux D., Muñoz M., Bulet P., and BachèrePenaeidins E. A family of antimicrobial peptides from penaeid shrimp (Crustacea, Decapoda). Cell Mol Life Sci 57 (2000) 1260-1271
47. Muñoz M., Vandenbulcke F., Saulnier D., and Bachère E. Expression and distribution of penaeidin antimicrobial peptides are regulated by haemocyte reactions in microbial challenged shrimp. Eur J Biochem 269 (2002) 2678-2689
48. Sequeira T., Tavares D., and Arala-Chaves M. Evidence for circulating hemocyte proliferation in the shrimp Penaeus japonicus. Dev Comp Immunol 20 (1996) 97-104
49. van de Braak C.B., Botterblom M.H., Liu W., Taverne N., van der Knaap W.P., and Rombout J.H. The role of the haematopoietic tissue in haemocyte production and maturation in the black tiger shrimp (Penaeus monodon). Fish Shellfish Immunol 12 (2002) 253-272
50. Bachère E., Gueguen Y., Gonzalez M., de Lorgeril J., Garnier J., and Romestand B. Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol Rev 198 (2004) 149-168
51. Noga E.J., Engel D.P., Arroll T.W., McKenna S., and Davidian M. Low serum antibacterial activity coincides with increased prevalence of shell disease in blue crabs Callinectes sapidus. Dis Aquat Org 19 (1994) 121-128
52. Le Moullac G., Soyez C., Saulnier D., Ansquer D., Avarre J.C., and Levy P. Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. Fish Shellfish Immunol 8 (1998) 621-629
53. McMahon B.R. Respiratory and circulatory compensation to hypoxia in crustaceans. Respir Physiol 128 (2001) 349-364
54. McMahon B.R., and Burnett L.E. The crustacean open circulatory system: a reexamination. Physiol Zool 63 (1990) 35-71
55. McMahon BR, Chu KH, Mak EMT. Development in the heart in the shrimp, Metapenaeus ensis. Fish and shellfish larvae culture symposium 1995: pp. 470-3.
56. Airriess C.N., and McMahon B.R. Cardiovascular adaptations enhance tolerance of environmental hypoxia in the crab, Cancer magister. J Exp Biol 190 (1994) 23-41
57. Nooteboom A., Bleichrodt R.P., and Hendriks T. Modulation of endothelial monolayer permeability induced by plasma obtained from lipopolysaccharide-stimulated whole blood. Clin Exp Immunol 144 (2006) 362-369